Modular switches shift monarch butterfly migratory flight behavior at their Mexican overwintering sites.

Eastern North American migratory monarch butterflies exhibit migratory behavioral states in fall and spring characterized by sun-dependent oriented flight. However, it is unclear how monarchs transition between these behavioral states at their overwintering site. Using a modified Mouritsen-Frost flight simulator, we confirm individual directionality and compass-based orientation (leading to group orientation) in fall migrants, and also uncover sustained flight propensity and direction-based flight reinforcement as distinctly migratory behavioral traits. By testing monarchs at their Mexican overwintering sites, we show that overwintering monarchs show reduced propensity for sustained flight and lose individual directionality, leading to the loss of group-level orientation. Overwintering fliers orient axially in a time-of-day dependent manner, which may indicate local versus long-distance directional heading. These results support a model of migratory flight behavior in which modular, state-dependent switches for flight propensity and orientation control are highly dynamic and are controlled in season- and location-dependent manners.

Model Systems in Ecology, Evolution, and Behavior: A Call for Diversity in Our Model Systems and Discipline.

AbstractEcologists and evolutionary biologists are fascinated by life's variation but also seek to understand phenomena and mechanisms that apply broadly across taxa. Model systems can help us extract generalities from amid all the wondrous diversity, but only if we choose and develop them carefully, use them wisely, and have a range of model systems from which to choose. In this introduction to the Special Feature on Model Systems in Ecology, Evolution, and Behavior (EEB), we begin by grappling with the question, What is a model system? We then explore where our model systems come from, in terms of the skills and other attributes required to develop them and the historical biases that influence traditional model systems in EEB. We emphasize the importance of communities of scientists in the success of model systems-narrow scientific communities can restrict the model organisms themselves. We also consider how our discipline was built around one type of "model scientist"-a history still reflected in the field. This lack of diversity in EEB is unjust and also narrows the field's perspective, including by restricting the questions asked and talents used to answer them. Increasing diversity, equity, and inclusion will require acting at many levels, including structural changes. Diversity in EEB, in both model systems and the scientists who use them, strengthens our discipline.

Monarch Butterfly Migration as an Integrative Model of Complex Trait Evolution.

AbstractUnderstanding the genetic architecture of complex trait adaptation in natural populations requires the continued development of tractable models that explicitly confront organismal and environmental complexity. A decade of high-throughput sequencing-based investigations into the genomic basis of migration points to an integrative framework that incorporates quantitative genetics, evolutionary developmental biology, phenotypic plasticity, and epigenetics to explain migration evolution. In this perspective, I argue that the transcontinental migration of the monarch butterfly (Danaus plexippus) can serve as a compelling system to study the mechanism of evolutionary lability of a complex trait. Monarchs show significant phenotypic and genotypic diversity across their global range, with phenotypic switching that allows for explicit study of evolutionary lability. A developmental approach for elucidating how migratory traits are generated and functionally integrated will be important for understanding the evolution of monarch migration traits. I propose a plasticity threshold model to describe migration lability, and I describe novel functional techniques that will help resolve open questions and model assumptions. I conclude by considering the relationships between adaptive genetic architecture, anthropogenic climate change, and conservation management practice and the timeliness of the monarch migration model to illuminate these connections given the rapid decline of the North American migration.

Monarch butterflies use an environmentally sensitive, internal timer to control overwintering dynamics.

The monarch butterfly (Danaus plexippus) complements its iconic migration with diapause, a hormonally controlled developmental programme that contributes to winter survival at overwintering sites. Although timing is a critical adaptive feature of diapause, how environmental cues are integrated with genetically-determined physiological mechanisms to time diapause development, particularly termination, is not well understood. In a design that subjected western North American monarchs to different environmental chamber conditions over time, we modularized constituent components of an environmentally-controlled, internal diapause termination timer. Using comparative transcriptomics, we identified molecular controllers of these specific diapause termination components. Calcium signalling mediated environmental sensitivity of the diapause timer, and we speculate that it is a key integrator of environmental condition (cold temperature) with downstream hormonal control of diapause. Juvenile hormone (JH) signalling changed spontaneously in diapause-inducing conditions, capacitating response to future environmental condition. Although JH is a major target of the internal timer, it is not itself the timer. Epigenetic mechanisms are implicated to be the proximate timing mechanism. Ecdysteroid, JH, and insulin/insulin-like peptide signalling are major targets of the diapause programme used to control response to permissive environmental conditions. Understanding the environmental and physiological mechanisms of diapause termination sheds light on fundamental properties of biological timing, and also helps inform expectations for how monarch populations may respond to future climate change.

BMP signaling is required for the generation of primordial germ cells in an insect.

Two modes of germ cell formation are known in animals. Specification through maternally inherited germ plasm occurs in many well-characterized model organisms, but most animals lack germ plasm by morphological and functional criteria. The only known alternative mechanism is induction, experimentally described only in mice, which specify germ cells through bone morphogenetic protein (BMP) signal-mediated induction of a subpopulation of mesodermal cells. Until this report, no experimental evidence of an inductive germ cell signal for specification has been available outside of vertebrates. Here we provide functional genetic experimental evidence consistent with a role for BMP signaling in germ cell formation in a basally branching insect. We show that primordial germ cells of the cricket Gryllus bimaculatus transduce BMP signals and require BMP pathway activity for their formation. Moreover, increased BMP activity leads to ectopic and supernumerary germ cells. Given the commonality of BMP signaling in mouse and cricket germ cell induction, we suggest that BMP-based germ cell formation may be a shared ancestral mechanism in animals.

Insulin signalling underlies both plasticity and divergence of a reproductive trait in Drosophila.

Phenotypic plasticity is the ability of a single genotype to yield distinct phenotypes in different environments. The molecular mechanisms linking phenotypic plasticity to the evolution of heritable diversification, however, are largely unknown. Here, we show that insulin/insulin-like growth factor signalling (IIS) underlies both phenotypic plasticity and evolutionary diversification of ovariole number, a quantitative reproductive trait, in Drosophila. IIS activity levels and sensitivity have diverged between species, leading to both species-specific ovariole number and species-specific nutritional plasticity in ovariole number. Plastic range of ovariole number correlates with ecological niche, suggesting that the degree of nutritional plasticity may be an adaptive trait. This demonstrates that a plastic response conserved across animals can underlie the evolution of morphological diversity, underscoring the potential pervasiveness of plasticity as an evolutionary mechanism.

Convergent evolution of a reproductive trait through distinct developmental mechanisms in Drosophila.

Convergent morphologies often arise due to similar selective pressures in independent lineages. It is poorly understood whether the same or different developmental genetic mechanisms underlie such convergence. Here we show that independent evolution of a reproductive trait, ovariole number, has resulted from changes in distinct developmental mechanisms, each of which may have a different underlying genetic basis in Drosophila. Ovariole number in Drosophila is species-specific, highly variable, and largely under genetic control. Convergent changes in Drosophila ovariole number have evolved independently within and between species. We previously showed that the number of a specific ovarian cell type, terminal filament (TF) cells, determines ovariole number. Here we examine TF cell development in different Drosophila lineages that independently evolved a significantly lower ovariole number than the D. melanogaster Oregon R strain. We show that in these Drosophila lineages, reduction in ovariole number occurs primarily through variations in one of two different developmental mechanisms: (1) reduced number of somatic gonad precursors (SGP cells) specified during embryogenesis; or (2) alterations of somatic gonad cell morphogenesis and differentiation in larval life. Mutations in the D. melanogaster Insulin Receptor (InR) alter SGP cell number but not ovarian morphogenesis, while targeted loss of function of bric-à-brac 2 (bab2) affects morphogenesis without changing SGP cell number. Thus, evolution can produce similar ovariole numbers through distinct developmental mechanisms, likely controlled by different genetic mechanisms.

Counting in oogenesis.

The determination of a precise number of cells within a structure and of a precise number of cellular structures within an organ is critical for correct development in animals and plants. However, relatively little is known about the molecular mechanisms that ensure that these numbers are achieved. We discuss counting mechanisms that operate during ovarian development and oogenesis.